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Functional analysis of potato genes involved in quantitative resistance to Phytophthora infestans

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Abstract

The most significant threat to potato production worldwide is the late blight disease, which is caused by the oomycete pathogen Phytophthora infestans. Based on previous cDNA microarrays and cDNA-amplified fragment length polymorphism analysis, 63 candidate genes that are expected to contribute to developing a durable resistance to late blight were selected for further functional analysis. We performed virus-induced gene silencing (VIGS) to these candidate genes on both Nicotiana benthamiana and potato, subsequently inoculated detached leaves and assessed the resistance level. Ten genes decreased the resistance to P. infestans after VIGS treatment. Among those, a lipoxygenase (LOX; EC 1.13.11.12) and a suberization-associated anionic peroxidase affected the resistance in both N. benthamiana and potato. Our results identify genes that may play a role in quantitative resistance mechanisms to late blight.

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Abbreviations

AFLP:

Amplified fragment length polymorphism

VIGS:

Virus-induced gene silencing

TRV:

Tobacco rattle virus

PVX:

Potato virus X

EST:

Expressed sequence tag

TDF:

Transcript derived fragments

BABA:

dl-β-amino-butyric acid

ORF:

Open reading frame

ANOVA:

Analysis of variance

REML:

Restricted maximum likelihood

SSH:

Suppression subtractive hybridization

LGR:

Lesion growth rate

PTGS:

Post-transcriptional gene silencing

PCR:

Polymerase chain reaction

NCBI:

National Center for Biotechnology Information

LOX:

Lipoxygenase

PGSC:

Potato Genome Sequencing Consortium

References

  1. Fry W (2008) Phytophthora infestans: the plant (and R gene) destroyer. Mol Plant Pathol 9(3):385–402. doi:10.1111/J.1364-3703.2007.00465.X

    Article  PubMed  Google Scholar 

  2. Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, Cano LM, Grabherr M, Kodira CD, Raffaele S, Torto-Alalibo T, Bozkurt TO, Ah-Fong AMV, Alvarado L, Anderson VL, Armstrong MR, Avrova A, Baxter L, Beynon J, Boevink PC, Bollmann SR, Bos JIB, Bulone V, Cai GH, Cakir C, Carrington JC, Chawner M, Conti L, Costanzo S, Ewan R, Fahlgren N, Fischbach MA, Fugelstad J, Gilroy EM, Gnerre S, Green PJ, Grenville-Briggs LJ, Griffith J, Grunwald NJ, Horn K, Horner NR, Hu CH, Huitema E, Jeong DH, Jones AME, Jones JDG, Jones RW, Karlsson EK, Kunjeti SG, Lamour K, Liu ZY, Ma LJ, MacLean D, Chibucos MC, McDonald H, McWalters J, Meijer HJG, Morgan W, Morris PF, Munro CA, O’Neill K, Ospina-Giraldo M, Pinzon A, Pritchard L, Ramsahoye B, Ren QH, Restrepo S, Roy S, Sadanandom A, Savidor A, Schornack S, Schwartz DC, Schumann UD, Schwessinger B, Seyer L, Sharpe T, Silvar C, Song J, Studholme DJ, Sykes S, Thines M, van de Vondervoort PJI, Phuntumart V, Wawra S, Weide R, Win J, Young C, Zhou SG, Fry W, Meyers BC, van West P, Ristaino J, Govers F, Birch PRJ, Whisson SC, Judelson HS, Nusbaum C (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461(7262):393–398. doi:10.1038/Nature08358

    Article  PubMed  CAS  Google Scholar 

  3. McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379. doi:10.1146/annurev.phyto.40.120501.101443

    Article  PubMed  CAS  Google Scholar 

  4. Van Der Plank JE (1971) Stability of resistance to Phytophthora infestans in cultivars without R genes. Potato Res 14(4):263–270. doi:10.1007/BF02355989

    Article  Google Scholar 

  5. Colon LT, Turkensteen LJ, Prummel W, Budding DJ, Hoogendoorn J (1995) Durable resistance to late blight (Phytophthora-infestans) in old potato cultivars. Eur J Plant Pathol 101(4):387–397. doi:10.1007/bf01874852

    Article  Google Scholar 

  6. Gyetvai G, Sonderkaer M, Gobel U, Basekow R, Ballvora A, Imhoff M, Kersten B, Nielsen KL, Gebhardt C (2012) The transcriptome of compatible and incompatible interactions of potato (Solanum tuberosum) with Phytophthora infestans revealed by DeepSAGE analysis. PLoS ONE 7(2):e31526. doi:10.1371/journal.pone.0031526

    Article  PubMed  CAS  Google Scholar 

  7. Tian ZD, Liu J, Xie CH (2003) Isolation of resistance related-genes to Phytophthora infestans with suppression subtractive hybridization in the R-gene-free potato. Acta Genet Sin 30(7):597–605

    PubMed  CAS  Google Scholar 

  8. Li YJ, Tian ZD, Liu J, Xie CH (2009) Comparative cDNA-AFLP analysis reveals that dl-beta-amino-butyric acid induces resistance through early activation of the host-defense genes in potato. Physiol Plantarum 136(1):19–29. doi:10.1111/j.1399-3054.2009.01209.x

    Article  CAS  Google Scholar 

  9. Andreu AB, Guevara MG, Wolski EA, Daleol GR, Caldiz DO (2006) Enhancement of natural disease resistance in potatoes by chemicals. Pest Manag Sci 62(2):162–170. doi:10.1002/Ps.1142

    Article  PubMed  CAS  Google Scholar 

  10. Cohen YR (2002) Beta-aminobutyric acid-induced resistance against plant pathogens. Plant Dis 86(6):691–692

    CAS  Google Scholar 

  11. Si-Ammour A, Mauch-Mani B, Mauch F (2003) Quantification of induced resistance against Phytophthora species expressing GFP as a vital marker: beta-aminobutyric acid but not BTH protects potato and Arabidopsis from infection. Mol Plant Pathol 4(4):237–248. doi:10.1046/J.1364-3703.2003.00168.X

    Article  PubMed  CAS  Google Scholar 

  12. Cohen YR (2002) Beta-aminobutyric acid-induced resistance against plant pathogens. Plant Dis 86(5):448–457. doi:10.1094/PDIS.2002.86.5.448

    Article  CAS  Google Scholar 

  13. Baulcombe DC (1999) Fast forward genetics based on virus-induced gene silencing. Curr Opin Plant Biol 2(2):109–113. doi:10.1016/S1369-5266(99)80022-3

    Article  PubMed  CAS  Google Scholar 

  14. Purkayastha A, Dasgupta I (2009) Virus-induced gene silencing: a versatile tool for discovery of gene functions in plants. Plant Physiol Biochem 47(11–12):967–976. doi:10.1016/j.plaphy.2009.09.001

    Article  PubMed  CAS  Google Scholar 

  15. Restrepo S, Myers KL, del Pozo O, Martin GB, Hart AL, Buell CR, Fry WE, Smart CD (2005) Gene profiling of a compatible interaction between Phytophthora infestans and Solanum tuberosum suggests a role for carbonic anhydrase. Mol Plant Microbe Interact 18(9):913–922. doi:10.1094/MPMI-18-0913

    Article  PubMed  CAS  Google Scholar 

  16. Liu YL, Schiff M, Marathe R, Dinesh-Kumar SP (2002) Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J 30(4):415–429. doi:10.1046/j.1365-313X.2002.01297.x

    Article  PubMed  CAS  Google Scholar 

  17. Ratcliff F, Martin-Hernandez AM, Baulcombe DC (2001) Tobacco rattle virus as a vector for analysis of gene function by silencing. Plant J 25(2):237–245. doi:10.1046/j.0960-7412.2000.00942.x

    Article  PubMed  CAS  Google Scholar 

  18. Goodin MM, Zaitlin D, Naidu RA, Lommel SA (2008) Nicotiana benthamiana: its history and future as a model for plant-pathogen interactions. Mol Plant Microbe Interact 21(8):1015–1026. doi:10.1094/Mpmi-21-8-1015

    Article  PubMed  CAS  Google Scholar 

  19. Faivre-Rampant O, Gilroy EM, Hrubikova K, Hein I, Millam S, Loake GJ, Birch P, Taylor M, Lacomme C (2004) Potato virus X-induced gene silencing in leaves and tubers of potato. Plant Physiol 134(4):1308–1316. doi:10.1104/pp.103.037507

    Article  PubMed  CAS  Google Scholar 

  20. Brigneti G, Martin-Hernandez AM, Jin HL, Chen J, Baulcombe DC, Baker B, Jones JDG (2004) Virus-induced gene silencing in Solanum species. Plant J 39(2):264–272. doi:10.1111/j.1365-313X.2004.02122.x

    Article  PubMed  CAS  Google Scholar 

  21. Wang BL, Liu J, Tian ZD, Song BT, Xie CH (2005) Monitoring the expression patterns of potato genes associated with quantitative resistance to late blight during Phytophthora infestans infection using cDNA microarrays. Plant Sci 169(6):1155–1167. doi:10.1016/j.plantsci.2005.07.020

    Article  CAS  Google Scholar 

  22. Xu X, Pan SK, Cheng SF, Zhang B, Mu DS, Ni PX, Zhang GY, Yang S, Li RQ, Wang J, Orjeda G, Guzman F, Torres M, Lozano R, Ponce O, Martinez D, De la Cruz G, Chakrabarti SK, Patil VU, Skryabin KG, Kuznetsov BB, Ravin NV, Kolganova TV, Beletsky AV, Mardanov AV, Di Genova A, Bolser DM, Martin DMA, Li GC, Yang Y, Kuang HH, Hu Q, Xiong XY, Bishop GJ, Sagredo B, Mejia N, Zagorski W, Gromadka R, Gawor J, Szczesny P, Huang SW, Zhang ZH, Liang CB, He J, Li Y, He Y, Xu JF, Zhang YJ, Xie BY, Du YC, Qu DY, Bonierbale M, Ghislain M, Herrera MD, Giuliano G, Pietrella M, Perrotta G, Facella P, O’Brien K, Feingold SE, Barreiro LE, Massa GA, Diambra L, Whitty BR, Vaillancourt B, Lin HN, Massa A, Geoffroy M, Lundback S, DellaPenna D, Buell CR, Sharma SK, Marshall DF, Waugh R, Bryan GJ, Destefanis M, Nagy I, Milbourne D, Thomson SJ, Fiers M, Jacobs JME, Nielsen KL, Sonderkaer M, Iovene M, Torres GA, Jiang JM, Veilleux RE, Bachem CWB, de Boer J, Borm T, Kloosterman B, van Eck H, Datema E, Hekkert BTL, Goverse A, van Ham RCHJ, Visser RGF, Consortiu PGS (2011) Genome sequence and analysis of the tuber crop potato. Nature 475(7355):189–195. doi:10.1038/Nature10158

    Article  PubMed  CAS  Google Scholar 

  23. Liu YL, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. Plant J 31(6):777–786. doi:10.1046/j.1365-313X.2002.01394.x

    Article  PubMed  CAS  Google Scholar 

  24. Vleeshouwers VGAA, van Dooijeweert W, Keizer LCP, Sijpkes L, Govers F, Colon LT (1999) A laboratory assay for Phytophthora infestans resistance in various Solanum species reflects the field situation. Eur J Plant Pathol 105(3):241–250. doi:10.1023/A:1008710700363

    Article  Google Scholar 

  25. Siedow JN (1991) Plant lipoxygenase—structure and function. Annu Rev Plant Phys 42:145–188. doi:10.1146/annurev.arplant.42.1.145

    Article  CAS  Google Scholar 

  26. Sembdner G, Parthier B (1993) The biochemistry and the physiological and molecular actions of jasmonates. Annu Rev Plant Phys 44:569–589. doi:10.1146/annurev.pp.44.060193.003033

    Article  CAS  Google Scholar 

  27. Kolomiets MV, Chen H, Gladon RJ, Braun EJ, Hannapel DJ (2000) A leaf lipoxygenase of potato induced specifically by pathogen infection. Plant Physiol 124(3):1121–1130. doi:10.1104/pp.124.3.1121

    Article  PubMed  CAS  Google Scholar 

  28. Mohan R, Kolattukudy PE (1990) Differential activation of expression of a suberization-associated anionic peroxidase gene in near-isogenic resistant and susceptible tomato lines by elicitors of verticillium-albo-atratrum. Plant Physiol 92(1):276–280. doi:10.1104/pp.92.1.276

    Article  PubMed  CAS  Google Scholar 

  29. Molina A, Mena M, Carbonero P, GarciaOlmedo F (1997) Differential expression of pathogen-responsive genes encoding two types of glycine-rich proteins in barley. Plant Mol Biol 33(5):803–810. doi:10.1023/A:1005712803130

    Article  PubMed  CAS  Google Scholar 

  30. Lagrimini LM, Gingas V, Finger F, Rothstein S, Liu TTY (1997) Characterization of antisense transformed plants deficient in the tobacco anionic peroxidase. Plant Physiol 114(4):1187–1196. doi:10.1104/pp.114.4.1187

    PubMed  CAS  Google Scholar 

  31. Burget EG, Verma R, Molhoj M, Reiter WD (2003) The biosynthesis of l-arabinose in plants: molecular cloning and characterization of a golgi-localized UDP-D-xylose 4-epimerase encoded by the MUR4 gene of Arabidopsis. Plant Cell 15(2):523–531. doi:10.1105/Tpc.008425

    Article  PubMed  CAS  Google Scholar 

  32. Aist JR (1976) Papillae and related wound plugs of plant-cells. Annu Rev Phytopathol 14:145–163. doi:10.1146/annurev.py.14.090176.001045

    Article  Google Scholar 

  33. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26(4):403–410. doi:10.1038/82521

    Article  PubMed  CAS  Google Scholar 

  34. Borrone JW, Kuhn DN, Schnell RJ (2004) Isolation, characterization, and development of WRKY genes as useful genetic markers in Theobroma cacao. Theor Appl Genet 109(3):495–507. doi:10.1007/s00122-004-1662-4

    Article  PubMed  CAS  Google Scholar 

  35. Cao H, Li X, Dong XN (1998) Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance. Proc Natl Acad Sci USA 95(11):6531–6536. doi:10.1073/pnas.95.11.6531

    Article  PubMed  CAS  Google Scholar 

  36. Vleeshouwers VGAA, Van Dooijeweert W, Govers F, Kamoun S, Colon LT (2000) Does basal PR gene expression in Solanum species contribute to non-specific resistance to Phytophthora infestans? Physiol Mol Plant Pathol 57(1):35–42. doi:10.1006/pmpp.2000.0278

    Article  CAS  Google Scholar 

  37. Ishihama N, Yamada R, Yoshioka M, Katou S, Yoshioka H (2011) Phosphorylation of the Nicotiana benthamiana WRKY8 transcription factor by MAPK functions in the defense response. Plant Cell 23(3):1153–1170. doi:10.1105/tpc.110.081794

    Article  PubMed  CAS  Google Scholar 

  38. Tian ZD, Liu J, Portal L, Bonierbale M, Xie CH (2008) Mapping of candidate genes associated with late blight resistance in potato and comparison of their location with known quantitative trait loci. Can J Plant Sci 88(4):599–610. doi:10.4141/CJPS07034

    Article  CAS  Google Scholar 

  39. Gebhardt C, Valkonen JPT (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39:79–102. doi:10.1146/annurev.phyto.39.1.79

    Article  PubMed  CAS  Google Scholar 

  40. Pajerowska-Mukhtar K, Stich B, Achenbach U, Ballvora A, Lubeck J, Strahwald J, Tacke E, Hofferbert HR, Ilarionova E, Bellin D, Walkemeier B, Basekow R, Kersten B, Gebhardt C (2009) Single nucleotide polymorphisms in the Allene Oxide Synthase 2 gene are associated with field resistance to late blight in populations of tetraploid potato cultivars. Genetics 181(3):1115–1127. doi:10.1534/genetics.108.094268

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Dr. Yajun Li for help with the construction of TRV: TDFs recombinants. Dr. Dinesh-Kumar is acknowledged for providing the TRV vectors. The work is partially supported by the Natural Science Foundation of Hubei Province (2010CDA102), the Earmarked Fund for Modern Agro-industry Technology Research System (CARS-10-P06) and China Scholarship Council Program for Graduate Students.

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  1. Xiaolei Shi

    Present address: Institute of Cereal and Oil Crops, Hebei Academy of Agriculture and Forestry Sciences, Shijiazhuang, 050031, People’s Republic of China

Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Biology (Huazhong Agricultural University), Ministry of Education, National Center for Vegetable Improvement (Central China), Potato Engineering and Technology Research Center of Hubei Province, Huazhong Agricultural University, Wuhan, 430070, Hubei, People’s Republic of China

    Juan Du, Zhendong Tian, Jun Liu, Xiaolei Shi & Conghua Xie

  2. Wageningen UR Plant Breeding, Wageningen University, P.O. Box 386, 6700 AJ, Wageningen, The Netherlands

    Juan Du & Vivianne G. A. A. Vleeshouwers

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  1. Juan Du
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  2. Zhendong Tian
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Correspondence to Conghua Xie.

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Du, J., Tian, Z., Liu, J. et al. Functional analysis of potato genes involved in quantitative resistance to Phytophthora infestans . Mol Biol Rep 40, 957–967 (2013). https://doi.org/10.1007/s11033-012-2137-3

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